The choroid plexus (ChP) produces cerebrospinal fluid and forms an essential brain barrier. ChP tissues form in each brain ventricle, each one adopting a distinct shape, but remarkably little is known about the mechanisms underlying ChP development. Here, we show that epithelial WNT5A is crucial for determining fourth ventricle (4V) ChP morphogenesis and size in mouse. Systemic Wnt5a knockout, or forced Wnt5a overexpression beginning at embryonic day 10.5, profoundly reduced ChP size and development. However, Wnt5a expression was enriched in Foxj1-positive epithelial cells of 4V ChP plexus, and its conditional deletion in these cells affected the branched, villous morphology of the 4V ChP. We found that WNT5A was enriched in epithelial cells localized to the distal tips of 4V ChP villi, where WNT5A acted locally to activate non-canonical WNT signaling via ROR1 and ROR2 receptors. During 4V ChP development, MEIS1 bound to the proximal Wnt5a promoter, and gain- and loss-of-function approaches demonstrated that MEIS1 regulated Wnt5a expression. Collectively, our findings demonstrate a dual function of WNT5A in ChP development and identify MEIS transcription factors as upstream regulators of Wnt5a in the 4V ChP epithelium.

Czech Centre for Phenogenomics and Laboratory of Transgenic Models of Diseases Institute of Molecular Genetics of the CAS Prague 142 20 Czech Republic

Department of Biochemistry and Functional Genomics Faculty of Medicine and Health Sciences Université de Sherbrooke Sherbrooke QC 75281 Canada

Department of Experimental Biology Faculty of Science Masaryk University Brno 61137 Czech Republic

Department of Medical Biochemistry and Biophysics Karolinska Institutet Stockholm 171 77 Sweden

Department of Pathology Boston Children's Hospital Boston MA 02115 USA

John van Geest Centre for Brain Repair and WT MRC Cambridge Stem Cell Centre University of Cambridge Cambridge CB2 0PY UK

Laboratory of Transcriptional Regulation Institute of Molecular Genetics of the CAS Prague 142 20 Czech Republic

Research Center on Aging CIUSSS de l'Estrie CHUS Sherbrooke QC 75361 Canada

Science for Life Laboratory Department of Biochemistry and Biophysics Stockholm University Solna SE 106 91 Sweden

Shanghai Institute of Cardiovascular Diseases Zhongshan Hospital Institutes of Biomedical Sciences Fudan University Shanghai 200032 China

Swammerdam Institute for Life Sciences Section of Molecular Cytology Faculty of Science University of Amsterdam1098 XH Netherlands

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Development. 2022 Feb 1;149(3):dev200517. doi: 10.1242/dev.200517. PubMed

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Alexander, C. M., Goel, S., Fakhraldeen, S. A. and Kim, S. (2012). Wnt signaling in mammary glands: plastic cell fates and combinatorial signaling. Cold Spring Harb. Perspect. Biol. 4, a008037. 10.1101/cshperspect.a008037 PubMed DOI PMC

Amin, S., Donaldson, I. J., Zannino, D. A., Hensman, J., Rattray, M., Losa, M., Spitz, F., Ladam, F., Sagerström, C. and Bobola, N. (2015). Hoxa2 selectively enhances meis binding to change a branchial arch ground state. Dev. Cell 32, 265-277. 10.1016/j.devcel.2014.12.024 PubMed DOI PMC

Awatramani, R., Soriano, P., Rodriguez, C., Mai, J. J. and Dymecki, S. M. (2003). Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat. Genet. 35, 70-75. 10.1038/ng1228 PubMed DOI

Bryja, V., Schulte, G., Rawal, N., Grahn, A. and Arenas, E. (2007). Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J. Cell Sci. 120, 586-595. 10.1242/jcs.03368 PubMed DOI

Carvalho, J. R., Fortunato, I. C., Fonseca, C. G., Pezzarossa, A., Barbacena, P., Dominguez-Cejudo, M. A., Vasconcelos, F. F., Santos, N. C., Carvalho, F. A. and Franco, C. A. (2019). Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration. eLife 8, e45853. 10.7554/eLife.45853 PubMed DOI PMC

Cervantes, S., Yamaguchi, T. P. and Hebrok, M. (2009). Wnt5a is essential for intestinal elongation in mice. Dev. Biol. 326, 285-294. 10.1016/j.ydbio.2008.11.020 PubMed DOI PMC

Chau, K. F., Springel, M. W., Broadbelt, K. G., Park, H., Topal, S., Lun, M. P., Mullan, H., Maynard, T., Steen, H., LaMantia, A. S.et al. (2015). Progressive differentiation and instructive capacities of amniotic fluid and cerebrospinal fluid proteomes following neural tube closure. Dev. Cell 35, 789-802. 10.1016/j.devcel.2015.11.015 PubMed DOI PMC

Chen, X., He, Y., Tian, Y., Wang, Y., Wu, Z., Lan, T., Wang, H., Cheng, K. and Xie, P. (2020). Different serotypes of adeno-associated virus vector- and lentivirus-mediated tropism in choroid plexus by intracerebroventricular delivery. Hum. Gene Ther. 31, 440-447. 10.1089/hum.2019.300 PubMed DOI

Choi, S.-C. and Sokol, S. Y. (2009). The involvement of lethal giant larvae and Wnt signaling in bottle cell formation in Xenopus embryos. Dev. Biol. 336, 68-75. 10.1016/j.ydbio.2009.09.033 PubMed DOI PMC

Cui, J., Shipley, F. B., Shannon, M. L., Alturkistani, O., Dani, N., Webb, M. D., Sugden, A. U., Andermann, M. L. and Lehtinen, M. K. (2020). Inflammation of the embryonic choroid plexus barrier following maternal immune activation. Dev. Cell 55, 617-628.e6. 10.1016/j.devcel.2020.09.020 PubMed DOI PMC

Currle, D. S., Cheng, X., Hsu, C.-M. and Monuki, E. S. (2005). Direct and indirect roles of CNS dorsal midline cells in choroid plexus epithelia formation. Development 132, 3549-3559. 10.1242/dev.01915 PubMed DOI

Dani, N., Herbst, R. H., McCabe, C., Green, G. S., Kaiser, K., Head, J. P., Cui, J., Shipley, F. B., Jang, A., Dionne, D.et al. (2021). A cellular and spatial map of the choroid plexus across brain ventricles and ages. Cell S0092-8674, 00438-4. 10.1016/j.cell.2021.04.003 PubMed DOI PMC

Dibner, C., Elias, S. and Frank, D. (2001). XMeis3 protein activity is required for proper hindbrain patterning in Xenopus laevis embryos. Development 128, 3415-3426. PubMed

Diez-Roux, G., Banfi, S., Sultan, M., Geffers, L., Anand, S., Rozado, D., Magen, A., Canidio, E., Pagani, M., Peluso, I.et al. (2011). A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol. 9, e1000582. 10.1371/journal.pbio.1000582 PubMed DOI PMC

Donaldson, I. J., Amin, S., Hensman, J. J., Kutejova, E., Rattray, M., Lawrence, N., Hayes, A., Ward, C. M. and Bobola, N. (2012). Genome-wide occupancy links Hoxa2 to Wnt–β-catenin signaling in mouse embryonic development. Nucleic Acids Res. 40, 3990-4001. 10.1093/nar/gkr1240 PubMed DOI PMC

Elkouby, Y. M., Polevoy, H., Gutkovich, Y. E., Michaelov, A. and Frank, D. (2012). A hindbrain-repressive Wnt3a/Meis3/Tsh1 circuit promotes neuronal differentiation and coordinates tissue maturation. Development 139, 1487-1497. 10.1242/dev.072934 PubMed DOI

Fame, R. M. and Lehtinen, M. K. (2020). Emergence and developmental roles of the cerebrospinal fluid system. Dev. Cell 52, 261-275. 10.1016/j.devcel.2020.01.027 PubMed DOI

Fumoto, K., Takigawa-Imamura, H., Sumiyama, K., Kaneiwa, T. and Kikuchi, A. (2017). Modulation of apical constriction by Wnt signaling is required for lung epithelial shape transition. Development 144, 151-162. 10.1242/dev.141325 PubMed DOI

Gao, B., Song, H., Bishop, K., Elliot, G., Garrett, L., English, M. A., Andre, P., Robinson, J., Sood, R., Minami, Y.et al. (2011). Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 20, 163-176. 10.1016/j.devcel.2011.01.001 PubMed DOI PMC

Ghersi-Egea, J.-F., Strazielle, N., Catala, M., Silva-Vargas, V., Doetsch, F. and Engelhardt, B. (2018). Molecular anatomy and functions of the choroidal blood-cerebrospinal fluid barrier in health and disease. Acta Neuropathol. 135, 337-361. 10.1007/s00401-018-1807-1 PubMed DOI

Gou, L., Ren, X. and Ji, P. (2021). Canonical Wnt signaling regulates branching morphogenesis of submandibular gland by modulating levels of lama5. Int. J. Dev. Biol. (in press). 10.1387/ijdb.200307lg PubMed DOI

Grosse, A. S., Pressprich, M. F., Curley, L. B., Hamilton, K. L., Margolis, B., Hildebrand, J. D. and Gumucio, D. L. (2011). Cell dynamics in fetal intestinal epithelium: Implications for intestinal growth and morphogenesis. Development 138, 4423-4432. 10.1242/dev.065789 PubMed DOI PMC

Grove, E. A., Tole, S., Limon, J., Yip, L. and Ragsdale, C. W. (1998). The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125, 2315-2325. PubMed

Grumolato, L., Liu, G., Mong, P., Mudbhary, R., Biswas, R., Arroyave, R., Vijayakumar, S., Economides, A. N. and Aaronson, S. A. (2010). Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 24, 2517-2530. 10.1101/gad.1957710 PubMed DOI PMC

Haddad, M. R., Donsante, A., Zerfas, P. and Kaler, S. G. (2013). Fetal brain-directed AAV gene therapy results in rapid, robust, and persistent transduction of mouse choroid plexus epithelia. Mol. Ther. Nucleic Acids 2, e101. 10.1038/mtna.2013.27 PubMed DOI PMC

Ho, H.-Y. H., Susman, M. W., Bikoff, J. B., Ryu, Y. K., Jonas, A. M., Hu, L., Kuruvilla, R. and Greenberg, M. E. (2012). Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc. Natl. Acad. Sci. USA 109, 1-8. 10.1073/iti0112109 PubMed DOI PMC

Hovanes, K., Li, T. W. H., Munguia, J. E., Truong, T., Milovanovic, T., Lawrence Marsh, J., Holcombe, R. F. and Waterman, M. L. (2001). β -catenin – sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28, 53-57. 10.1038/ng0501-53 PubMed DOI

Huang, L., Pu, Y., Hu, W. Y., Birch, L., Luccio-Camelo, D., Yamaguchi, T. and Prins, G. S. (2009). The role of Wnt5a in prostate gland development. Dev. Biol. 328, 188-199. 10.1016/j.ydbio.2009.01.003 PubMed DOI PMC

Humphries, A. C. and Mlodzik, M. (2018). From instruction to output: Wnt/PCP signaling in development and cancer. Curr. Opin. Cell Biol. 51, 110-116. 10.1016/j.ceb.2017.12.005 PubMed DOI PMC

Hunter, N. L. and Dymecki, S. M. (2007). Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus. Development 134, 3449-3460. 10.1242/dev.003095 PubMed DOI PMC

Jho, E.-H., Zhang, T., Domon, C., Joo, C.-K., Freund, J.-N. and Costantini, F. (2002). Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183. PubMed PMC

Johansson, P. A., Irmler, M., Acampora, D., Beckers, J., Simeone, A. and Götz, M. (2013). The transcription factor Otx2 regulates choroid plexus development and function. Development 140, 1055-1066. 10.1242/dev.090860 PubMed DOI

Kaiser, K., Gyllborg, D., Procházka, J., Salašová, A., Kompaníková, P., Molina, F. L., Laguna-Goya, R., Radaszkiewicz, T., Harnoš, J., Procházková, M.et al. (2019). WNT5A is transported via lipoprotein particles in the cerebrospinal fluid to regulate hindbrain morphogenesis. Nat. Commun. 10, 1-15. 10.1038/s41467-019-09298-4 PubMed DOI PMC

Kallay, L. M., McNickle, A., Brennwald, P. J., Hubbard, A. L. and Braiterman, L. T. (2006). Scribble associates with two polarity proteins, Lgl2 and Vangl2, via distinct molecular domains. J. Cell. Biochem. 99, 647-664. 10.1002/jcb.20992 PubMed DOI

Kato, M., Soprano, D. R., Makover, A., Kato, K., Herbert, J. and Goodman, D. W. S. (1986). Localization of immunoreactive transthyretin (prealbumin) and of transthyretin mRNA in fetal and adult rat brain. Differentiation 31, 228-235. 10.1111/j.1432-0436.1986.tb00402.x PubMed DOI

Kessenbrock, K., Smith, P., Steenbeek, S. C., Pervolarakis, N., Kumar, R., Minami, Y., Goga, A., Hinck, L. and Werb, Z. (2017). Diverse regulation of mammary epithelial growth and branching morphogenesis through noncanonical Wnt signaling. Proc. Natl. Acad. Sci. USA 114, 3121-3126. 10.1073/pnas.1701464114 PubMed DOI PMC

Kumawat, K. and Gosens, R. (2015). WNT-5A: signaling and functions in health and disease. Cell. Mol. Life Sci. 73, 567-587. 10.1007/s00018-015-2076-y PubMed DOI PMC

Langford, M. B., O'Leary, C. J., Veeraval, L., White, A., Lanoue, V. and Cooper, H. M. (2020). WNT5a regulates epithelial morphogenesis in the developing choroid plexus. Cereb. Cortex 30, 3617-3631. 10.1093/cercor/bhz330 PubMed DOI

Langmead, B., Trapnell, C., Pop, M. and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25. 10.1186/gb-2009-10-3-r25 PubMed DOI PMC

Laurent, B., Ruitu, L., Murn, J., Hempel, K., Ferrao, R., Xiang, Y., Liu, S., Garcia, B. A., Wu, H., Wu, F.et al. (2015). A specific LSD1/KDM1A isoform regulates neuronal differentiation through H3K9 demethylation. Mol. Cell 57, 957-970. 10.1016/j.molcel.2015.01.010 PubMed DOI PMC

Lehtinen, M. K., Zappaterra, M. W., Chen, X., Yang, Y. J., Hill, A. D., Lun, M., Maynard, T., Gonzalez, D., Kim, S., Ye, P.et al. (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69, 893-905. 10.1016/j.neuron.2011.01.023 PubMed DOI PMC

Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J.et al. (2006). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176. 10.1038/nature05453 PubMed DOI

Lewis, A. E., Vasudevan, H. N., O'Neill, A. K., Soriano, P. and Bush, J. O. (2013). The widely used Wnt1-Cre transgene causes developmental phenotypes by ectopic activation of Wnt signaling. Dev. Biol. 379, 229-234. 10.1016/j.ydbio.2013.04.026 PubMed DOI PMC

Li, C., Hu, L., Xiao, J., Chen, H., Li, J. T., Bellusci, S., Delanghe, S. and Minoo, P. (2005). Wnt5a regulates Shh and Fgf10 signaling during lung development. Dev. Biol. 287, 86-97. 10.1016/j.ydbio.2005.08.035 PubMed DOI

Liddelow, S. A., Dziegielewska, K. M., VandeBerg, J. L. and Saunders, N. R. (2010). Development of the lateral ventricular choroid plexus in a marsupial, Monodelphis domestica. Cerebrospinal Fluid Res. 7, 16. 10.1186/1743-8454-7-16 PubMed DOI PMC

Lun, M. P., Johnson, M. B., Broadbelt, K. G., Watanabe, M., Kang, Y.-J., Chau, K. F., Springel, M. W., Malesz, A., Sousa, A. M. M., Pletikos, M.et al. (2015). Spatially heterogeneous choroid plexus transcriptomes encode positional identity and contribute to regional CSF production. J. Neurosci. 35, 4903-4916. 10.1523/JNEUROSCI.3081-14.2015 PubMed DOI PMC

Machon, O., Masek, J., Machonova, O., Krauss, S. and Kozmik, Z. (2015). Meis2 is essential for cranial and cardiac neural crest development. BMC Dev. Biol. 15, 40. 10.1186/s12861-015-0093-6 PubMed DOI PMC

Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R.et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140. 10.1038/nn.2467 PubMed DOI PMC

Mentink, R. A., Rella, L., Radaszkiewicz, T. W., Gybel, T., Betist, M. C., Bryja, V. and Korswagen, H. C. (2018). The planar cell polarity protein VANG-1/Vangl negatively regulates Wnt/β-catenin signaling through a Dvl dependent mechanism. PLoS Genet. 14, e1007840. 10.1371/journal.pgen.1007840 PubMed DOI PMC

Mercader, N., Selleri, L., Criado, L. M., Pallares, P., Parras, C., Cleary, M. L. and Torres, M. (2009). Ectopic Meis1 expression in the mouse limb bud alters P-D patterning in a Pbx1-independent manner. Int. J. Dev. Biol. 53, 1483-1494. 10.1387/ijdb.072430nm PubMed DOI

Muthusamy, N., Vijayakumar, A., Cheng, G. and Ghashghaei, H. T. (2014). A Knock-in Foxj1CreERT2:: GFP mouse for recombination in epithelial cells with motile cilia. Genesis 52, 350-358. 10.1002/dvg.22753 PubMed DOI PMC

Nakamura, E., Nguyen, M.-T. and Mackem, S. (2006). Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreERT to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 235, 2603-2612. 10.1002/dvdy.20892 PubMed DOI

Niehrs, C. (2012). The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol. 13, 767-779. 10.1038/nrm3470 PubMed DOI

Nielsen, C. M. and Dymecki, S. M. (2010). Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. Dev. Biol. 340, 430-437. 10.1016/j.ydbio.2010.01.032 PubMed DOI PMC

Philipp, I., Aufschnaiter, R., Ozbek, S., Pontasch, S., Jenewein, M., Watanabe, H., Rentzsch, F., Holstein, T. W. and Hobmayer, B. (2009). Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra. Proc. Natl. Acad. Sci. USA 106, 4290-4295. 10.1073/pnas.0812847106 PubMed DOI PMC

Pietilä, I., Prunskaite-Hyyryläinen, R., Kaisto, S., Tika, E., van Eerde, A. M., Salo, A. M., Garma, L., Miinalainen, I., Feitz, W. F., Bongers, E. M. H. F.et al. (2016). Wnt5a deficiency leads to anomalies in ureteric tree development, tubular epithelial cell organization and basement membrane integrity pointing to a role in kidney collecting duct patterning. PLoS ONE 11, e0147171. 10.1371/journal.pone.0147171 PubMed DOI PMC

Pourreyron, C., Reilly, L., Proby, C., Panteleyev, A., Fleming, C., McLean, K., South, A. P. and Foerster, J. (2012). Wnt5a is strongly expressed at the leading edge in non-melanoma skin cancer, forming active gradients, while canonical Wnt signalling is repressed. PLoS ONE 7, e31827. 10.1371/journal.pone.0031827 PubMed DOI PMC

Ramakrishnan, V. M., Tien, K. T., McKinley, T. R., Bocard, B. R., McCurry, T. M., Williams, S. K., Hoying, J. B. and Boyd, N. L. (2016). Wnt5a Regulates the Assembly of Human Adipose Derived Stromal Vascular Fraction-Derived Microvasculatures. PLoS ONE 11, e0151402. 10.1371/journal.pone.0151402 PubMed DOI PMC

Roarty, K., Baxley, S. E., Crowley, M. R., Frost, A. R. and Serra, R. (2009). Loss of TGF-β or Wnt5a results in an increase in Wnt/β-catenin activity and redirects mammary tumour phenotype. Breast Cancer Res. 11, R19. 10.1186/bcr2244 PubMed DOI PMC

Ryu, Y. K., Collins, S. E., Ho, H.-Y. H., Zhao, H. and Kuruvilla, R. (2013). An autocrine Wnt5a-Ror signaling loop mediates sympathetic target innervation. Dev. Biol. 377, 79-89. 10.1016/j.ydbio.2013.02.013 PubMed DOI PMC

Saito-Diaz, K., Chen, T. W., Wang, X., Thorne, C. A., Wallace, H. A., Page-McCaw, A. and Lee, E. (2013). The way Wnt works: components and mechanism. Growth Factors 31, 1-31. 10.3109/08977194.2012.752737 PubMed DOI PMC

Sato, A., Yamamoto, H., Sakane, H., Koyama, H. and Kikuchi, A. (2010). Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 29, 41-54. 10.1038/emboj.2009.322 PubMed DOI PMC

Silva-Vargas, V., Maldonado-Soto, A. R., Mizrak, D., Codega, P. and Doetsch, F. (2016). Age-dependent Niche signals from the choroid plexus regulate adult neural stem cells. Cell Stem Cell 19, 643-652. 10.1016/j.stem.2016.06.013 PubMed DOI

Sittaramane, V., Pan, X., Glasco, D. M., Huang, P., Gurung, S., Bock, A., Li, S., Wang, H., Kawakami, K., Matise, M. P.et al. (2013). The PCP protein Vangl2 regulates migration of hindbrain motor neurons by acting in floor plate cells, and independently of cilia function. Dev. Biol. 382, 400-412. 10.1016/j.ydbio.2013.08.017 PubMed DOI PMC

Stephens, W. Z., Senecal, M., Nguyen, M. and Piotrowski, T. (2010). Loss of adenomatous polyposis coli (apc) results in an expanded ciliary marginal zone in the zebrafish eye. Dev. Dyn. 239, 2066-2077. 10.1002/dvdy.22325 PubMed DOI

Sui, L. and Dahmann, C. (2020). Wingless counteracts epithelial folding by increasing mechanical tension at basal cell edges in Drosophila. Development 147, dev184713. 10.1242/dev.184713 PubMed DOI

Sun, M. Z., Oh, M. C., Ivan, M. E., Kaur, G., Safaee, M., Kim, J. M., Phillips, J. J., Auguste, K. I. and Parsa, A. T. (2014). Current management of choroid plexus carcinomas. Neurosurg. Rev. 37, 179-192. 10.1007/s10143-013-0499-1 PubMed DOI

Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J.-P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530. 10.1038/35035117 PubMed DOI

Topol, L., Jiang, X., Choi, H., Garrett-Beal, L., Carolan, P. J. and Yang, Y. (2003). Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J. Cell Biol. 162, 899-908. 10.1083/jcb.200303158 PubMed DOI PMC

van Amerongen, R., Fuerer, C. and Mizutani, M. (2012). Wnt5a can both activate and repress Wnt/β-catenin signaling during mouse embryonic development. Dev. Biol. 369, 101-114. 10.1016/j.ydbio.2012.06.020 PubMed DOI PMC

Wilting, J. and Christ, B. (1989). An experimental and ultrastructural study on the development of the avian choroid plexus. Cell Tissue Res. 255, 487-494. 10.1007/BF00218783 PubMed DOI

Xu, H., Fame, R. M., Sadegh, C., Sutin, J., Naranjo, C., Syau, C. D., Cui, J., Shipley, F. B., Vernon, A., Gao, F.et al. (2021). Choroid plexus NKCC1 mediates cerebrospinal fluid clearance during mouse early postnatal development. Nat. Commun. 12, 447. 10.1038/s41467-020-20666-3 PubMed DOI PMC

Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223. PubMed

Yamamoto, H., Yoo, S. K., Nishita, M., Kikuchi, A. and Minami, Y. (2007). Wnt5a modulates glycogen synthase kinase 3 to induce phosphorylation of receptor tyrosine kinase Ror2. Genes Cells 12, 1215-1223. 10.1111/j.1365-2443.2007.01128.x PubMed DOI

Yamamoto, H., Awada, C., Matsumoto, S., Kaneiwa, T., Sugimoto, T., Takao, T. and Kikuchi, A. (2015). Basolateral secretion of Wnt5a in polarized epithelial cells is required for apical lumen formation. J. Cell Sci. 128, 1051-1063. 10.1242/jcs.163683 PubMed DOI

Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nussbaum, C., Myers, R. M., Brown, M., Li, W.et al. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137. 10.1186/gb-2008-9-9-r137 PubMed DOI PMC

Zhu, L. J., Gazin, C., Lawson, N. D., Pagès, H., Lin, S. M., Lapointe, D. S. and Green, M. R. (2010). ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinformatics 11, 237. 10.1186/1471-2105-11-237 PubMed DOI PMC

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